Regulation of αβ/γδ T cell development by the activator protein 1 transcription factor c-Jun

Journal of Immunology

Volumn 178, Issue 9, 2007, Pages 5690-5700

  Riera Sans, Lluís ^a,b   Behrens, Axel ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; INTERLEUKIN 7 RECEPTOR ALPHA; MESSENGER RNA; PROTEIN C JUN; PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; INTEGRASE; INTERLEUKIN 7 RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL CYCLE; CELL DEATH; CELL SELECTION; CHIMERA; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE DELETION; LYMPHOPOIESIS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SPLEEN CELL; T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTEGRASES; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, INTERLEUKIN-7; T-LYMPHOCYTES; THYMUS GLAND;

EID: 34247637187     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.9.5690     Document Type: Article

References (61)

1. Warren, L. A., and E. V. Rothenberg. 2003. Regulatory coding of lymphoid lineage choice by hematopoietic transcription factors. Curr. Opin. Immunol. 15: 166-175.
2. Rodewald, H. R., and H. J. Fehling. 1998. Molecular and cellular events in early thymocyte development. Adv. Immunol. 69: 1-112.
3. Berg, L. J., and J. Kang. 2001. Molecular determinants of TCR expression and selection. Curr. Opin. Immunol. 13: 232-241.
4. Sim, G. K., C. Olsson, and A. Augustin. 1995. Commitment and maintenance of the αβ and γδ T cell lineages. J. Immunol. 154: 5821-5831.
5. Schweighoffer, E., and B. J. Fowlkes. 1996. Positive selection is not required for thymic maturation of transgenic γδ T cells. J. Exp. Med. 183: 2033-2041.
6. Terrence, K., C. P. Pavlovich, E. O. Matechak, and B. J. Fowlkes. 2000. Premature expression of T cell receptor (TCR) αβ suppresses TCRγδ gene rearrangement but permits development of γδ lineage T cells. J. Exp. Med. 192: 537-548.
7. Haks, M. C., J. M. Lefebvre, J. P. Lauritsen, M. Carleton, M. Rhodes, T. Miyazaki, D. J. Kappes, and D. L. Wiest. 2005. Attenuation of γδTCR signaling efficiently diverts thymocytes to the αβ lineage. Immunity 22: 595-606.
8. Hayes, S. M., L. Li, and P. E. Love. 2005. TCR signal strength influences αβ/γδ lineage fate. Immunity 22: 583-593.
9. Fehling, H. J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptor α gene in development of αβ but not γδ T cells. Nature 375: 795-798.
10. Malissen, M., A. Gillet, L. Ardouin, G. Bouvier, J. Trucy, P. Ferrier, E. Vivier, and B. Malissen. 1995. Altered T cell development in mice with a targeted mutation of the CD3-ε gene. EMBO J. 14: 4641-4653.
11. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
12. Mombaerts, P., A. R. Clarke, M. A. Rudnicki, J. Iacomini, S. Itohara, J. J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M. L. Hooper, et al. 1992. Mutations in T-cell antigen receptor genes α and β block thymocyte development at different stages. Nature 360: 225-231.
13. Mombaerts, P., J. Iacomini, R. S. Johnson, K. Herrup, S. Tonegawa, and V. E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
14. Haks, M. C., P. Krimpenfort, J. Borst, and A. M. Kruisbeek. 1998. The CD3γ chain is essential for development of both the TCRαβ and TCRγδ lineages. EMBO J. 17: 1871-1882.
15. Dave, V. P., Z. Cao, C. Browne, B. Alarcon, G. Fernandez-Miguel, J. Lafaille, A. de la Hera, S. Tonegawa, and D. J. Kappes. 1997. CD3 δ deficiency arrests development of the αβ but not the γδ T cell lineage. EMBO J. 16: 1360-1370.
16. Peschon, J. J., P. J. Morrissey, K. H. Grabstein, F. J. Ramsdell, E. Maraskovsky, B. C. Gliniak, L. S. Park, S. F. Ziegler, D. E. Williams, C. B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180: 1955-1960.
17. von Freeden-Jeffry, U., P. Vieira, L. A. Lucian, T. McNeil, S. E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181: 1519-1526.
18. Maki, K., S. Sunaga, Y. Komagata, Y. Kodaira, A. Mabuchi, H. Karasuyama, K. Yokomuro, J. I. Miyazaki, and K. Ikuta. 1996. Interleukin 7 receptor-deficient mice lack γδ T cells. Proc. Natl. Acad. Sci. USA 93: 7172-7177.
19. -/- mice. J. Immunol. 157: 2366-2373.
20. Watanabe, Y., T. Sudo, N. Minato, A. Ohnishi, and Y. Katsura. 1991. Interleukin 7 preferentially supports the growth of γδ T cell receptor-bearing T cells from fetal thymocytes in vitro. Int. Immunol. 3: 1067-1075.
21. Kang, J., A. Volkmann, and D. H. Raulet. 2001. Evidence that γδ versus αβ T cell fate determination is initiated independently of T cell receptor signaling. J. Exp. Med. 193: 689-698.
22. Jochum, W., E. Passegue, and E. F. Wagner. 2001. AP-1 in mouse development and tumorigenesis. Oncogene 20: 2401-2412.
23. Angel, P., and M. Karin. 1991. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochem. Biophys. Acta 1072: 129-157.
24. Mechta-Grigoriou, F., D. Gerald, and M. Yaniv. 2001. The mammalian Jun proteins: redundancy and specificity. Oncogene 20: 2378-2389.
25. Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
26. Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP1. Cell 55: 875-885.
27. Sabapathy, K., Y. Hu, T. Kallunki, M. Schreiber, J. P. David, W. Jochum, E. F. Wagner, and M. Karin. 1999. JNK2 is required for efficient T-cell activation and apoptosis but not for normal lymphocyte development. Curr. Biol. 9: 116-125.
28. 2-terminal kinase (JNK)1 and JNK2 have similar and stage-dependent roles in regulating T cell apoptosis and proliferation. J. Exp. Med. 193: 317-328.
29. Dong, C., D. D. Yang, C. Tournier, A. J. Whitmarsh, J. Xu, R. J. Davis, and R. A. Flavell. 2000. JNK is required for effector T-cell function but not for T-cell activation. Nature 405: 91-94.
30. Dong, C., D. D. Yang, M. Wysk, A. J. Whitmarsh, R. J. Davis, and R. A. Flavell. 1998. Defective T cell differentiation in the absence of Jnk1. Science 282: 2092-2095.
31. + T cells to Th1 cells requires MAP kinase JNK2. Immunity 9: 575-585.
32. Hilberg, F., A. Aguzzi, N. Howells, and E. F. Wagner. 1993. c-jun is essential for normal mouse development and hepatogenesis. Nature 365: 179-181.
33. Johnson, R. S., B. van Lingen, V. E. Papaioannou, and B. M. Spiegelmann. 1993. A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev. 7: 1309-1317.
34. Chen, J., V. Stewart, G. Spyrou, F. Hilberg, E. F. Wagner, and F. W. Alt. 1994. Generation of normal T and B lymphocytes by c-jun deficient embryonic stem cells. Immunity 1: 65-72.
35. Williams, K. L., A. J. Zullo, M. H. Kaplan, R. R. Brutkiewicz, C. D. Deppmann, C. Vinson, and E. J. Taparowsky. 2003. BATF transgenic mice reveal a role for activator protein-1 in NKT cell development. J. Immunol. 170: 2417-2426.
36. Thornton, T. M., A. J. Zullo, K. L. Williams, and E. J. Taparowsky. 2006. Direct manipulation of activator protein-1 controls thymocyte proliferation in vitro. Eur. J. Immunol. 36: 160-169.
37. + thymocytes. Int. Immunol. 11: 1203-1216.
38. Behrens, A., M. Sibilia, and E. F. Wagner. 1999. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21: 326-329.
39. Behrens, A., K. Sabapathy, I. Graef, M. Geary, G. R. Crabtree, and E. F. Wagner. 2001. Jun N-terminal kinase 2 modulates thymocyte apoptosis and T cell activation through c-Jun and nuclear factor of activated T cell (NF-AT). Proc. Natl. Acad. Sci. USA 98: 1769-1774.
40. Behrens, A., M. Sibilia, J. P. David, U. Mohle-Steinlein, F. Tranche, G. Schutz, and E. F. Wagner. 2002. Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver. EMBO J. 21: 1782-1790.
41. Takahama, Y., K. Ohishi, Y. Tokoro, T. Sugawara, Y. Yoshimura, M. Okabe, T. Kinoshita, and J. Takeda. 1998. Functional competence of T cells in the absence of glycosylphpsphatidylinositol-anchored proteins caused by T cell-specific disruption of the Pig-a gene. Eur. J. Immunol. 28: 2159-2166.
42. Spangrude, G. J. 1994. Biological and clinical aspects of hematopoietic stem cells. Annu. Rev. Med. 45: 93-104.
43. Nateri, A. S., B. Spencer-Dene, and A. Behrens. 2005. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285.
44. Fischer, A. M., C. D. Katayama, G. Pages, J. Pouyssegur, and S. M. Hedrick. 2005. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 23: 431-443.
45. Wilson, A., M. Capone, and H. R. MacDonald. 1999. Unexpectedly late expression of intracellular CD3ε and TCR γδ proteins during adult thymus development. Int. Immunol. 11: 1641-1650.
46. Eferl, R., and E. F. Wagner. 2003. AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3: 859-868.
47. Tanigaki, K., M. Tsuji, N. Yamamoto, H. Han, J. Tsukada, H. Inoue, M. Kubo, and T. Honjo. 2004. Regulation of αβ/γδ T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 20: 611-622.
48. Washburn, T., E. Schweighoffer, T. Gridley, D. Chang, B. J. Fowlkes, D. Cado, and E. Robey. 1997. Notch activity influences the αβ versus γδ T cell lineage decision. Cell 88: 833-843.
49. 2/M cell-cycle progression and cellular senescence. Nat. Cell Biol. 6: 215-226.
50. Okada, S., Z. Q. Wang, A. E. Grigoriadis, E. F. Wagner, and T. von Ruden. 1994. Mice lacking c-fos have normal hematopoietic stem cells but exhibit altered B-cell differentiation due to an impaired bone marrow environment. Mol. Cell. Biol. 14: 382-390.
51. Meixner, A., F. Karreth, L. Kenner, and E. F. Wagner. 2004. JunD regulates lymphocyte proliferation and T helper cell cytokine expression. EMBO J. 23: 1325-1335.
52. Hartenstein, B., S. Teurich, J. Hess, J. Schenkel, M. Schorpp-Kistner, and P. Angel. 2002. Th2 cell-specific cytokine expression and allergen-induced airway inflammation depend on JunB. EMBO J. 21: 6321-6329.
53. Pennington, D. J., B. Silva-Santos, and A. C. Hayday. 2005. γδ T cell development: having the strength to get there. Curr. Opin. Immunol. 17: 108-115.
54. Yu, Q., B. Erman, J. H. Park, L. Feigenbaum, and A. Singer. 2004. IL-7 receptor signals inhibit expression of transcription factors TCF-1, LEF-1, and RORγt: impact on thymocyte development. J. Exp. Med. 200: 797-803.
55. Hoffmann, R., L. Bruno, T. Seidl, A. Rolink, and F. Melchers. 2003. Rules for gene usage inferred from a comparison of large-scale gene expression profiles of T and B lymphocyte development. J. Immunol. 170: 1339-1353.
56. Allman, D., A. Sambandam, S. Kim, J. P. Miller, A. Pagan, D. Well, A. Meraz, and A. Bhandoola. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4: 168-174.
57. Porritt, H. E., L. L. Rumfelt, S. Tabrizifard, T. M. Schmitt, J. C. Zuniga-Pflucker, and H. T. Petrie. 2004. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20: 735-745.
58. Maki, K., S. Sunaga, and K. Ikuta. 1996. The V-J recombination of T cell receptor-γ genes is blocked in interleukin-7 receptor-deficient mice. J. Exp. Med. 184: 2423-2427.
59. Schlissel, M. S., S. D. Durum, and K. Muegge. 2000. The interleukin 7 receptor is required for T cell receptor γ locus accessibility to the V(D)J recombinase. J. Exp. Med. 191: 1045-1050.
60. Durum, S. K., S. Candeias, H. Nakajima, W. J. Leonard, A. M. Baird, L. J. Berg, and K. Muegge. 1998. Interleukin 7 receptor control of T cell receptor γ gene rearrangement: role of receptor-associated chains and locus accessibility. J. Exp. Med. 188: 2233-2241.
61. Kang, J., M. Coles, and D. H. Raulet. 1999. Defective development of γ/δ T cells in interleukin 7 receptor-deficient mice is due to impaired expression of T cell receptor γ genes. J. Exp. Med. 190: 973-982.